Systems-wide analysis of the ROK-family regulatory gene rokL6 and its role in the control of glucosamine toxicity in Streptomyces coelicolor
Central metabolism plays a key role in the control of growth and antibiotic production in streptomycetes. Specifically, aminosugars act as signaling molecules that affect development and antibiotic production, via metabolic interference with the global repressor DasR. While aminosugar metabolism dir...
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| Veröffentlicht in: | Applied and environmental microbiology 2023-12, Vol.89 (12), p.e0167423-e0167423 |
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| creator | Li, Chao Urem, Mia Du, Chao Zhang, Le van Wezel, Gilles P |
| description | Central metabolism plays a key role in the control of growth and antibiotic production in streptomycetes. Specifically, aminosugars act as signaling molecules that affect development and antibiotic production, via metabolic interference with the global repressor DasR. While aminosugar metabolism directly connects to other major metabolic routes such as glycolysis and cell wall synthesis, several important aspects of their metabolism are yet unresolved. Accumulation of
-acetylglucosamine 6-phosphate or glucosamine 6-phosphate is lethal to many bacteria, a yet unresolved phenomenon referred to as "aminosugar sensitivity." We made use of this concept by selecting for suppressors in genes related to glucosamine toxicity in
mutants, which showed that the gene pair of
-family regulatory gene
and major facilitator superfamily transporter gene sco1448 forms a cryptic rescue mechanism. Inactivation of
resulted in the expression of sco1448, which then prevents the toxicity of amino sugar-derived metabolites in
. The systems biology of RokL6 and its transcriptional control of sco1448 shed new light on aminosugar metabolism in streptomycetes and on the response of bacteria to aminosugar toxicity. |
| doi_str_mv | 10.1128/aem.01674-23 |
| format | Article |
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-acetylglucosamine 6-phosphate or glucosamine 6-phosphate is lethal to many bacteria, a yet unresolved phenomenon referred to as "aminosugar sensitivity." We made use of this concept by selecting for suppressors in genes related to glucosamine toxicity in
mutants, which showed that the gene pair of
-family regulatory gene
and major facilitator superfamily transporter gene sco1448 forms a cryptic rescue mechanism. Inactivation of
resulted in the expression of sco1448, which then prevents the toxicity of amino sugar-derived metabolites in
. The systems biology of RokL6 and its transcriptional control of sco1448 shed new light on aminosugar metabolism in streptomycetes and on the response of bacteria to aminosugar toxicity.</description><identifier>ISSN: 0099-2240</identifier><identifier>EISSN: 1098-5336</identifier><identifier>DOI: 10.1128/aem.01674-23</identifier><identifier>PMID: 37982622</identifier><language>eng</language><publisher>United States: American Society for Microbiology</publisher><subject>Amino Sugars - metabolism ; Anti-Bacterial Agents ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Bacteriology ; Bioinformatics ; Cellulose ; Chitin ; Chitosan ; Gene Expression Regulation, Bacterial ; Gene sequencing ; Genes, Regulator ; Genetics ; Genetics and Molecular Biology ; Glucosamine ; Glucosamine - metabolism ; Maltose ; Metabolic pathways ; Metabolites ; Mutants ; N-Acetylglucosamine ; Polysaccharides ; Saccharides ; Streptomyces - genetics ; Streptomyces coelicolor - genetics ; Streptomyces coelicolor - metabolism ; Streptomycetes ; Systems analysis ; Toxicity</subject><ispartof>Applied and environmental microbiology, 2023-12, Vol.89 (12), p.e0167423-e0167423</ispartof><rights>Copyright © 2023 American Society for Microbiology.</rights><rights>Copyright American Society for Microbiology Dec 2023</rights><rights>Copyright © 2023 American Society for Microbiology. 2023 American Society for Microbiology.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-a366t-496a0fb608d1ae54cb0dbdbb4c61e85037cb57f4e452950c965bfc3dcf1867233</cites><orcidid>0000-0003-3447-5293 ; 0000-0003-0341-1561 ; 0000-0002-8062-4539</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://journals.asm.org/doi/pdf/10.1128/aem.01674-23$$EPDF$$P50$$Gasm2$$H</linktopdf><linktohtml>$$Uhttps://journals.asm.org/doi/full/10.1128/aem.01674-23$$EHTML$$P50$$Gasm2$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,3188,27924,27925,52751,52752,52753,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37982622$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Atomi, Haruyuki</contributor><creatorcontrib>Li, Chao</creatorcontrib><creatorcontrib>Urem, Mia</creatorcontrib><creatorcontrib>Du, Chao</creatorcontrib><creatorcontrib>Zhang, Le</creatorcontrib><creatorcontrib>van Wezel, Gilles P</creatorcontrib><title>Systems-wide analysis of the ROK-family regulatory gene rokL6 and its role in the control of glucosamine toxicity in Streptomyces coelicolor</title><title>Applied and environmental microbiology</title><addtitle>Appl Environ Microbiol</addtitle><addtitle>Appl Environ Microbiol</addtitle><description>Central metabolism plays a key role in the control of growth and antibiotic production in streptomycetes. Specifically, aminosugars act as signaling molecules that affect development and antibiotic production, via metabolic interference with the global repressor DasR. While aminosugar metabolism directly connects to other major metabolic routes such as glycolysis and cell wall synthesis, several important aspects of their metabolism are yet unresolved. Accumulation of
-acetylglucosamine 6-phosphate or glucosamine 6-phosphate is lethal to many bacteria, a yet unresolved phenomenon referred to as "aminosugar sensitivity." We made use of this concept by selecting for suppressors in genes related to glucosamine toxicity in
mutants, which showed that the gene pair of
-family regulatory gene
and major facilitator superfamily transporter gene sco1448 forms a cryptic rescue mechanism. Inactivation of
resulted in the expression of sco1448, which then prevents the toxicity of amino sugar-derived metabolites in
. The systems biology of RokL6 and its transcriptional control of sco1448 shed new light on aminosugar metabolism in streptomycetes and on the response of bacteria to aminosugar toxicity.</description><subject>Amino Sugars - metabolism</subject><subject>Anti-Bacterial Agents</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Bacteriology</subject><subject>Bioinformatics</subject><subject>Cellulose</subject><subject>Chitin</subject><subject>Chitosan</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>Gene sequencing</subject><subject>Genes, Regulator</subject><subject>Genetics</subject><subject>Genetics and Molecular Biology</subject><subject>Glucosamine</subject><subject>Glucosamine - metabolism</subject><subject>Maltose</subject><subject>Metabolic pathways</subject><subject>Metabolites</subject><subject>Mutants</subject><subject>N-Acetylglucosamine</subject><subject>Polysaccharides</subject><subject>Saccharides</subject><subject>Streptomyces - genetics</subject><subject>Streptomyces coelicolor - genetics</subject><subject>Streptomyces coelicolor - metabolism</subject><subject>Streptomycetes</subject><subject>Systems analysis</subject><subject>Toxicity</subject><issn>0099-2240</issn><issn>1098-5336</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kktv1DAURi0EokNhxxpFYgMSKX4nXiFUlYcYqRKFteU4N1MXJx5sB5r_wI_GM1PKQ2JlXfnco3v9GaHHBJ8QQtuXBsYTTGTDa8ruoBXBqq0FY_IuWmGsVE0px0foQUpXGGOOZXsfHbFGtVRSukI_LpaUYUz1d9dDZSbjl-RSFYYqX0L18fxDPZjR-aWKsJm9ySEu1QYmqGL4spaloa9cTqXyULlp32TDlEu9c2z8bEMqgtKQw7WzLi877CJH2OYwLhZS4cE7G3yID9G9wfgEj27OY_T5zdmn03f1-vzt-9PX69owKXPNlTR46CRue2JAcNvhvuu7jltJoBWYNbYTzcCBC6oEtkqKbrCstwNpZUMZO0avDt7t3I3QWygDG6-30Y0mLjoYp_--mdyl3oRvmuCGccGaYnh2Y4jh6wwp69ElC96bCcKcNG0VxQQL0Rb06T_oVZhjeehCKUIbprjihXpxoGwMKUUYbqchWO9y1iVnvc9Z7zd4fsBNGulv4X_YJ39ueyv-9QnYT25js8E</recordid><startdate>20231221</startdate><enddate>20231221</enddate><creator>Li, Chao</creator><creator>Urem, Mia</creator><creator>Du, Chao</creator><creator>Zhang, Le</creator><creator>van Wezel, Gilles P</creator><general>American Society for Microbiology</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7QO</scope><scope>7SN</scope><scope>7SS</scope><scope>7ST</scope><scope>7T7</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>SOI</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-3447-5293</orcidid><orcidid>https://orcid.org/0000-0003-0341-1561</orcidid><orcidid>https://orcid.org/0000-0002-8062-4539</orcidid></search><sort><creationdate>20231221</creationdate><title>Systems-wide analysis of the ROK-family regulatory gene rokL6 and its role in the control of glucosamine toxicity in Streptomyces coelicolor</title><author>Li, Chao ; Urem, Mia ; Du, Chao ; Zhang, Le ; van Wezel, Gilles P</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a366t-496a0fb608d1ae54cb0dbdbb4c61e85037cb57f4e452950c965bfc3dcf1867233</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Amino Sugars - metabolism</topic><topic>Anti-Bacterial Agents</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>Bacteriology</topic><topic>Bioinformatics</topic><topic>Cellulose</topic><topic>Chitin</topic><topic>Chitosan</topic><topic>Gene Expression Regulation, Bacterial</topic><topic>Gene sequencing</topic><topic>Genes, Regulator</topic><topic>Genetics</topic><topic>Genetics and Molecular Biology</topic><topic>Glucosamine</topic><topic>Glucosamine - metabolism</topic><topic>Maltose</topic><topic>Metabolic pathways</topic><topic>Metabolites</topic><topic>Mutants</topic><topic>N-Acetylglucosamine</topic><topic>Polysaccharides</topic><topic>Saccharides</topic><topic>Streptomyces - genetics</topic><topic>Streptomyces coelicolor - genetics</topic><topic>Streptomyces coelicolor - metabolism</topic><topic>Streptomycetes</topic><topic>Systems analysis</topic><topic>Toxicity</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Li, Chao</creatorcontrib><creatorcontrib>Urem, Mia</creatorcontrib><creatorcontrib>Du, Chao</creatorcontrib><creatorcontrib>Zhang, Le</creatorcontrib><creatorcontrib>van Wezel, Gilles P</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Applied and environmental microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Li, Chao</au><au>Urem, Mia</au><au>Du, Chao</au><au>Zhang, Le</au><au>van Wezel, Gilles P</au><au>Atomi, Haruyuki</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Systems-wide analysis of the ROK-family regulatory gene rokL6 and its role in the control of glucosamine toxicity in Streptomyces coelicolor</atitle><jtitle>Applied and environmental microbiology</jtitle><stitle>Appl Environ Microbiol</stitle><addtitle>Appl Environ Microbiol</addtitle><date>2023-12-21</date><risdate>2023</risdate><volume>89</volume><issue>12</issue><spage>e0167423</spage><epage>e0167423</epage><pages>e0167423-e0167423</pages><issn>0099-2240</issn><eissn>1098-5336</eissn><abstract>Central metabolism plays a key role in the control of growth and antibiotic production in streptomycetes. Specifically, aminosugars act as signaling molecules that affect development and antibiotic production, via metabolic interference with the global repressor DasR. While aminosugar metabolism directly connects to other major metabolic routes such as glycolysis and cell wall synthesis, several important aspects of their metabolism are yet unresolved. Accumulation of
-acetylglucosamine 6-phosphate or glucosamine 6-phosphate is lethal to many bacteria, a yet unresolved phenomenon referred to as "aminosugar sensitivity." We made use of this concept by selecting for suppressors in genes related to glucosamine toxicity in
mutants, which showed that the gene pair of
-family regulatory gene
and major facilitator superfamily transporter gene sco1448 forms a cryptic rescue mechanism. Inactivation of
resulted in the expression of sco1448, which then prevents the toxicity of amino sugar-derived metabolites in
. The systems biology of RokL6 and its transcriptional control of sco1448 shed new light on aminosugar metabolism in streptomycetes and on the response of bacteria to aminosugar toxicity.</abstract><cop>United States</cop><pub>American Society for Microbiology</pub><pmid>37982622</pmid><doi>10.1128/aem.01674-23</doi><tpages>23</tpages><orcidid>https://orcid.org/0000-0003-3447-5293</orcidid><orcidid>https://orcid.org/0000-0003-0341-1561</orcidid><orcidid>https://orcid.org/0000-0002-8062-4539</orcidid><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; American Society for Microbiology Journals; PubMed Central; Alma/SFX Local Collection |
| subjects | Amino Sugars - metabolism Anti-Bacterial Agents Bacterial Proteins - genetics Bacterial Proteins - metabolism Bacteriology Bioinformatics Cellulose Chitin Chitosan Gene Expression Regulation, Bacterial Gene sequencing Genes, Regulator Genetics Genetics and Molecular Biology Glucosamine Glucosamine - metabolism Maltose Metabolic pathways Metabolites Mutants N-Acetylglucosamine Polysaccharides Saccharides Streptomyces - genetics Streptomyces coelicolor - genetics Streptomyces coelicolor - metabolism Streptomycetes Systems analysis Toxicity |
| title | Systems-wide analysis of the ROK-family regulatory gene rokL6 and its role in the control of glucosamine toxicity in Streptomyces coelicolor |
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